Skip to main content
NCBI home page
Physiology and Molecular Biology of Plants logoLink to Physiology and Molecular Biology of Plants
. 2025 Jul 22;31(10):1705–1717. doi: 10.1007/s12298-025-01623-0

Genome-wide identification and expression analysis of the EgTCP transcription factor family in Eucalyptus grandis

Guiping Mou 1,2, Ran Xu 1,2, Jiayi Hu 1,2, Xiaodong Yan 1,2, Bing Zhang 3,✉
PMCID: PMC12559502  PMID: 41164119

Abstract

The TCP (Teosinte Branched 1/Cycloidea/Proliferating Cell Factors) transcription factor family plays a critical role in plant growth, development, and stress responses. To investigate the functions of the TCP gene family in Eucalyptus grandis (E. grandis), we performed a comprehensive genome-wide identification and analysis of E. grandis TCP (EgTCP) genes using bioinformatics approaches. We examined their expression patterns across different tissues and under salicylic acid (SA), jasmonic acid (JA), and salt stress conditions. Our analysis identified 15 TCP genes in the E. grandis genome, designated EgTCP1–EgTCP15. The encoded proteins range from 194 to 427 amino acid residues, with molecular weights between 21.68 and 44.90 kDa and isoelectric points spanning 6.45–0.41. Biochemical property predictions classified all EgTCP proteins as hydrophilic and unstable. Chromosomal mapping revealed that EgTCP genes are unevenly distributed across 11 chromosomes. Gene structure analysis indicated that EgTCP genes contain one to two exons and up to one intron. The presence of a highly conserved TCP domain was confirmed by conserved motif and phylogenetic analyses, which classified EgTCP proteins into three subfamilies: PCF, CIN, and CYC/TB1. Cis-regulatory element analysis of the promoter regions revealed multiple hormone-responsive and stress-related elements, suggesting potential regulatory roles in plant growth and abiotic stress adaptation. Expression profiling indicated that most EgTCP genes respond to SA and JA induction and exhibit tissue-specific expression patterns. The subcellular localization experiment indicated that EgTCP 13 was located in the nucleus. Overall, these findings provide valuable insights into the functional roles of the TCP gene family in E. grandis, establishing a foundation for future studies on their biological significance in plant growth, development, and stress tolerance.

Supplementary Information

The online version contains supplementary material available at 10.1007/s12298-025-01623-0.

Keywords: TCP gene family, Eucalyptus grandis, Stress responses, Phylogenetic analysis, Cis-regulatory elements

Introduction

The TCP (Teosinte Branched 1/Cycloidea/Proliferating Cell Factors) gene family encodes plant-specific transcription factors that originated in algae and mosses, progressively replicating and expanding during plant evolution to eventually form a multi-gene family (Nishiyama et al. 2018; Liu et al. 2019). TCP is a unique class of transcription factors in plants, named after the abbreviations of three genes: teosinte branched 1 (TB1) in maize (Zea mays) (Davis et al. 1999), cycloidea (CYC) in snapdragon (Antirrhinum majus) (Luo et al. 1996), and proliferating cell factor 1/2 (PCF1/2) in rice (Oryza sativa) (Kosugi and Ohashi 1997). The proteins of the TCP transcription factor family contain a highly conserved basic Helix-Loop-Helix (bHLH) domain at their N-terminus (Aggarwal et al. 2010). According to the distinct features of the TCP domain, TCP transcription factors can be divided into two subfamilies: Class I TCP and Class II TCP (Aggarwal et al. 2010; Horn et al. 2015). Class I TCP, also known as the PCF type, contains only one typical TCP conserved domain and is missing four amino acids (Martin-Trillo and Cubas 2010). Class II TCP can be further divided into the CIN subfamily and the CYC/TB1 subfamily, characterized by the insertion of four conserved amino acids in the TCP domain (Madrigal et al. 2017; Pabon-Mora et al. 2020). Members of the TCP gene family play crucial roles in various aspects of plant growth and development, hormone regulation, and response to abiotic stress and defense (Matus et al. 2003; Kolsch and Gleissberg 2006; Damerval et al. 2007; Aguilar-Martinez and Sinha 2013; Xu et al. 2013; Madrigal et al. 2017; Pabon-Mora et al. 2020; Zhao et al. 2021; Wang et al. 2023). They participate in regulating signal transduction, synthesis, and transport of various plant hormones to adapt to environmental influences on plant growth and development, as well as in protein interactions during hormone signaling processes (e.g., with SAP11 and MYB) to enhance plant resistance to stress (Nag et al. 2009; Giraud et al. 2010; Braun et al. 2012; Lopez et al. 2015). Moreover, the TCP gene family is also known to regulate processes such as seed germination, leaf and pollen development, cell cycle regulation, and cellular senescence in various plants (Giraud et al. 2010; Horn et al. 2015), including Arabidopsis (Arabidopsis thaliana) (Aggarwal et al. 2010), tomato (Solanum lycopersicum) (Parapunova et al. 2014), grape (Vitis vinifera) (Leng et al. 2019), foxtail millet (Setaria italic) (Xiong et al. 2022), and rice (Oryza sativa) (Minakuchi et al. 2010).

Previous studies have identified a total of 37 CsTCP genes in tea plants (Camellia sinensis) (Shang et al. 2022), and the results indicate that CsTCP proteins in different groups may have complementary functions, while proteins within the same class exhibit functional redundancy. There is no relationship between the number of CsTCP gene members and genome size, and the CsTCP gene family has only expanded since the divergence of monocots and eudicots. Chai et al. (2017) identified 29 TCP transcription factors in maize, discovering that they are distributed across 10 chromosomes and are highly conserved in evolution, with the highest expression of TCP genes in the maize ear and stem, indicating their involvement in growth regulation. In cotton (Gossypium raimondii), 38 TCP transcription factors were identified and divided into 11 subgroups based on phylogenetic relationships, unevenly distributed across 11 chromosomes, with the primary events of gene family replication being segmental duplications (Ma et al. 2014). Danisman et al. performed bioinformatics analysis on the protein sequence similarities and interactions of the 24 members of the Arabidopsis TCP transcription factor family, revealing functional redundancy between AtTCP19 and AtTCP20, which play roles in controlling leaf senescence (Danisman et al. 2013).

Eucalyptus grandis is a common fast-growing tree species belonging to the Myrtaceae family, widely distributed in Australia and surrounding areas, but it has now been introduced to other parts of the world. Its leaves are rich in fragrance and are often used to extract essential oils (Ridoutt and Pharis 1998; Costa et al. 2004; Medhurst and Beadle 2005; Zhao et al. 2019). Eucalyptus grandis has a rapid growth rate and can survive in poor soils and arid environments, and in some regions, it can improve soil quality. Although the genome of E. grandis has been reported, there has been no systematic analysis of the TCP gene family in E. grandis to date. This study employed bioinformatics methods to search the E. grandis genome database and identified 15 members of the TCP gene family, which are distributed across all chromosomes. Phylogenetic analysis indicated that the TCP gene family in E. grandis can be classified into the PCF, CYC/TB1, and CIN subfamilies. Additionally, analysis of the E. grandis TCP protein structures revealed that all TCP members contain a conserved TCP domain. By analyzing the promoter sequences of the E. grandis TCP genes, we discovered various cis-regulatory elements related to environmental response, hormone signaling, and growth and development. Expression pattern analysis showed that most members of the E. grandis TCP gene family exhibited tissue specificity, indicating that these genes are likely to play important roles in the regulation of growth and development. This study systematically conducted evolutionary and expression analyses of the E. grandis TCP gene family, and these results will provide valuable reference information for further research on gene function and breeding work in E. grandis.

Materials and methods

Identification and physiochemical properties analysis of EgTCP genes in E. grandis

We obtained the E. grandis genome and GFF files from the E. grandis genome database (https://bar.utoronto.ca/eplant_eucalyptus). We utilized TBtools software to extract the coding DNA sequences (CDS) for E. grandis genes and translated the CDS into protein sequences. The protein sequences of the TCP gene family from Arabidopsis were downloaded from TAIR (https://www.Arabidopsis.org/). Using the “Blast Compare Two Sequence Files” tool in TBtools (Wang et al. 2003), we compared the protein sequences of the 24 TCP gene family members in Arabidopsis with the E. grandis protein sequences, identifying all potential TCP genes in the E. grandis genome. The hidden Markov model (HMM) of TCP transcription factors (ID: PF03634) was downloaded from the Pfam database (http://pfam-legacy.xfam.org/) to initially screen for candidate sequences containing TCP protein domains. SMART (http://smart.embl.de, accessed on 1 June 2024) and NCBI’s CDD (https://www.ncbi.nlm.nih.gov/cdd, accessed on 1 June 2024) were used for further confirmation of AcTCP transcription factors with completly conserved domains. The remaining genes were designated as members of the E. grandis TCP family, resulting in a total of 15 TCP gene sequences. Constructing a phylogenetic tree using the neighbor-joining method in MEGAX software (Kumar et al. 2018). We used the online tool ExPASy (https://www.expasy.org/tools) to predict the number of amino acids, relative molecular weight (MW), and theoretical isoelectric point (PI) of EcTCPs. The hydrophobicity of the proteins was analyzed using Expasy (https://web.expasy.org/protscale/, accessed on 1 June 2024), and SOPMA (https://npsa-prabi.ibcp.fr/cgi-bin/npsa_automat.pl?page=npsa_sopma.html, accessed on 1 June 2024) was utilized for secondary structure prediction.

Chromosome localization of EgTCP gene family in E. grandis

The chromosome localization information of all members of the E. grandis TCP gene family was downloaded from the E. grandis genome database (https://bar.utoronto.ca/eplant_eucalyptus). Based on their localization information, the 15 members of the E. grandis TCP gene family were mapped onto the chromosomes using TBtools (Chen et al. 2023).

Gene structure and conserved motif analysis of EgTCP genes

The online MEME program version 5.0.5 (Bailey et al. 2015) (http://meme-suite.org/tools/meme, accessed on 1 June 2024) was used to predict the conserved motifs of the E. grandis TCP proteins, setting the motif length to be between 6 and 100 amino acids and the number of motifs to 10. Combined with the results of phylogenetic analysis, the gene structures and conserved motif diagrams were generated using TBtools (Chen et al. 2023).

Phylogenetic tree construction of EgTCP genes

A phylogenetic analysis was performed using the protein sequences of the 15 EgTCPs and other species TCPs (Arabidopsis, Oryza sativa, Citrus sinensis, Solanum lycopersicum, Populus trichocarpa). The neighbor-joining method was employed to construct the phylogenetic tree using MEGA software version 10.1.8 (Kumar et al. 2018) (https://www.megasoftware.net/, accessed on 1 June 2024), with parameters set as follows: Bootstrap Replications = 1000, Model/Method = p-distance, and Gap/Missing Data Treatment = Pairwise deletion. The clustering results were displayed using Evolview V3 (https://www.evolgenius.com).

Collinearity analysis

First, based on the annotation information of the E. grandis genome, we obtained the chromosomal localization information of the EgTCP family members and performed BLASTP (Li and Lu 2019) analysis on all protein sequences of E. grandis. Combining this with genome annotation information, we used MCScanX (V.1.1) (Wang et al. 2012) to analyze the tandem and segmental duplication relationships of genes in E. grandis. Similarly, MCScanX software was also employed for collinearity analysis of EgTCP genes across different species. We first identified all collinear regions between varieties and among species, and then selected the regions containing EgTCP genes. The homologous genes found in the collinear regions were considered direct homologs. The multiple synteny plot module in TBtools (V.2.031) was used to create collinearity maps between species and varieties.

Analysis of cis-acting elements in EgTCP gene promoters

The sequences of 2000 bp upstream of the transcription start sites of EgTCP family members were downloaded from the E. grandis genome database. Cis-acting element analysis was performed on the sequences upstream of translation start sites of the EgTCP genes using PlantCARE (http://bioinformatics.psb.ugent.be/webtools/plantcare/html/). Statistical analysis was conducted using R language software, and a heatmap of the cis-acting elements in the promoters was generated using TBtools (Chen et al. 2023).

Expression analysis of EgTCP genes

The spatiotemporal expression of genes reflects their functional characteristics to some extent. All the transcriptome data in this study were generated in the laboratory previously, and have been published (Fan et al. 2024) and uploaded to the database (National Geoscience Data Centre accession number: PRJCA002468, https://ngdc.cncb.ac.cn/search/specific?db=biosample&q=PRJCA002468). Additionally, we extracted the expression profiles of EgTCP genes from the transcriptome datasets by matching transcript IDs. Next, we extracted the FPKM values (Fragments Per Kilobase of exon model per Million mapped reads) for the EgTCP genes in different tissues. The FPKM values (+1) were then converted to log2 values, and a heatmap was generated using TBtools to analyze the expression patterns of the genes.

Subcellular localizationI

Through the seamless cloning technique, construct the pCAMBIA1302-EgTCP13-GFP fusion expression vector, and carry out co-localization analysis combined with the NLS-mCherry nuclear localization signal. The specific process includes: gene cloning: design specific primers containing 15–25 bp homologous arms, amplify the EgTCP13 gene using high-fidelity PCR (system: PrimeSTAR® Max premix, 50 μL reaction system, 30 cycles), double enzyme digestion (KpnI/BamHI) to linearize pCAMBIA1302-GFP (Driven by the CaMV 35S promoter) vector and purify it; vector construction: use Gibson Assembly® (10 μL system, 50 ng vector and 30 ng insert fragment, incubate at 50 °C for 30–60 min) to directionally ligate the target gene with the vecto. Then we transform DH5α competent cells, and screen positive clones through hygromycin resistance and sequencing verification. Next, we co-transfect the leaves of Nicotiana benthamiana with the recombinant plasmid and NLS-mCherry nuclear labeling vector using Agrobacterium tumefaciens infiltration method (GV3101 strain, OD600 = 0.8). Finally we capture dual-channel fluorescence signals using a confocal microscope (excitation wavelength GFP 488 nm/mCherry 587 nm) 48 h later.

Results

Identification and characterization of the EgTCP gene family in E. grandis

To identify TCP genes in E. grandis, we performed a genome-wide search using nucleotide sequences of TCP genes from A. thaliana as queries. This analysis led to the identification of 15 TCP genes in the E. grandis genome (Table 1). These genes were designated EgTCP1–EgTCP15. Physicochemical property analysis revealed that EgTCP proteins range in size from 194 to 427 amino acid residues, with molecular weights varying from 21.68 to 44.90 kDa and isoelectric points (pI) between 6.45 and 10.41. All EgTCP proteins exhibited negative GRAVY (grand average of hydropathy) values, indicating that they are hydrophilic. Subcellular localization predictions suggested that all EgTCP proteins are localized in the nucleus. To further investigate the phylogenetic relationships of the EgTCP gene family, we performed a phylogenetic analysis using MEGA software. The resulting phylogenetic tree (Fig. 1) clustered EgTCP proteins alongside TCP proteins from five other species (A. thaliana, Oryza sativa, Citrus sinensis, Solanum lycopersicum, and Populus trichocarpa). The clustering analysis classified EgTCP genes into three subfamilies: Class I (PCF subfamily) and Class II, which consists of the CIN and CYC/TB1 subfamilies. Among the 15 EgTCP proteins, the PCF subfamily contained the largest number of genes (seven members), whereas the CIN and CYC/TB1 subfamilies each contained four members. These findings suggest that the EgTCP gene family is evolutionarily conserved across plant species.

Table 1.

Analysis of the physicochemical characteristics of the eucalyptus EgTCP gene family

Sequence ID Name Number of amino acid Molecular weight Theoretical pI Instability index Aliphatic index Grand average of hydropathicity Subcellular localization
Eucgr.A01143.1.v2.0 EgTCP1 206 21,680.53 7.7 62.41 70.83 − 0.35 Nucleus
Eucgr.A02843.1.v2.0 EgTCP2 343 35,580.41 9.05 63.56 59.21 − 0.581 Nucleus
Eucgr.B00471.1.v2.0 EgTCP3 427 44,907.43 6.7 67.88 56.56 − 0.619 Nucleus
Eucgr.B00608.1.v2.0 EgTCP4 405 44,419.28 6.6 60.86 72.22 − 0.6 Nucleus
Eucgr.B00699.1.v2.0 EgTCP5 363 40,048.41 6.53 51.21 65.12 − 0.758 Nucleus
Eucgr.B03427.1.v2.0 EgTCP6 270 28,668.77 10.07 72.42 55.07 − 0.688 Nucleus
Eucgr.B03529.1.v2.0 EgTCP7 286 30,207.42 6.45 52.72 67.83 − 0.555 Nucleus
Eucgr.F01204.1.v2.0 EgTCP8 414 44,803.27 6.66 63.06 61.84 − 0.725 Nucleus
Eucgr.F02587.1.v2.0 EgTCP9 214 22,416.79 10.41 68.49 58.55 − 0.714 Nucleus
Eucgr.G02354.1.v2.0 EgTCP10 194 21,807.44 9.62 36.63 61.91 − 1.095 Nucleus
Eucgr.I02038.1.v2.0 EgTCP11 338 37,109.33 6.85 61.83 71.27 − 0.578 Nucleus
Eucgr.J01466.1.v2.0 EgTCP12 308 35,211.63 9.27 59.34 70.62 − 0.847 Nucleus
Eucgr.K01089.1.v2.0 EgTCP13 358 39,055.27 7.23 59.46 61.09 − 0.609 Nucleus
Eucgr.K02535.1.v2.0 EgTCP14 253 28,560.49 9.34 49.45 87.47 − 0.493 Nucleus
Eucgr.K02654.1.v2.0 EgTCP15 345 39,466.17 8.72 56.61 62.17 − 0.976 Nucleus
Open in a new tab

Fig. 1.

Fig. 1

Open in a new tab

Phylogenetic analysis of TCP family proteins. Oryza sativa (Os), Citrus (Cs), Arabidopsis thaliana (At), Solanum lycopersicum (Sl), Populus (Pe). Distinct colors and shapes are employed to distinguish between various species, with color-coded sections on the phylogenetic tree representing five distinct groups. CYC/TB1, CIN and PCF represent different subgroups

Structural analysis of the EgTCP gene family in E. grandis

To explore the structural features of EgTCP proteins, we identified 10 conserved motifs within their sequences. The motif distribution analysis (Fig. 2A) indicated that all EgTCP proteins contain conserved motifs characteristic of their respective subfamilies. Motif 1 was present in all EgTCP proteins, underscoring its evolutionary conservation. Additionally, Motif 2 was found exclusively in the PCF subfamily, while Motif 3 was specific to Class II (CIN and CYC/TB1 subfamilies). Furthermore, Motif 6 was unique to the CIN subfamily, and Motif 4 was specific to the CYC/TB1 subfamily. The similarity in motif composition among members of the same subfamily suggests conserved functional roles.

Fig. 2.

Fig. 2

Open in a new tab

Evolutionary tree and motif analysis A, conserved domains analysis B, and gene structure analysis C of EgTCPs

A conserved domain analysis (Fig. 2B) confirmed that all EgTCP proteins contain the signature TCP domain, essential for their transcriptional regulatory functions. Gene structure analysis (Fig. 2C) revealed that the EgTCP genes have relatively simple structures, consisting of coding sequences (CDS) with minimal intronic regions. Among the 15 EgTCP genes, 9 contained introns, while EgTCP6 was the only gene lacking untranslated regions (UTRs). These findings highlight the structural conservation of EgTCP genes, consistent with their roles in transcriptional regulation.

Chromosomal distribution of EgTCP genes

Following the identification of EgTCP genes, we mapped their chromosomal locations in the E. grandis genome. The chromosomal distribution analysis (Fig. 3) revealed that EgTCP genes are unevenly distributed across seven chromosomes, while four chromosomes do not contain any EgTCP genes. Chromosome 2 (Chr02) harbors the highest number of EgTCP genes (five members), whereas chromosomes Chr07 and Chr09 contain only a single EgTCP gene each. This non-uniform distribution suggests potential gene duplication events and chromosomal rearrangements during the evolution of the EgTCP gene family.

Fig. 3.

Fig. 3

Open in a new tab

Chromosomal localization of eucalyptus EgTCPs

Synteny analysis of the TCPs in different plants

To further investigate the evolutionary history of EgTCP genes, we conducted a comparative synteny analysis between E. grandis and five other species. The analysis (Fig. 4) revealed that E. grandis shares the fewest syntenic TCP gene pairs with pineapple (Ananas comosus), with only four pairs identified. In contrast, the highest number of syntenic gene pairs was observed between E. grandis and tomato (S. lycopersicum), indicating a relatively conserved evolutionary trajectory between these species. Further examination of syntenic regions suggested that during the evolutionary transition from tomato to E. grandis, most EgTCP genes were retained on chromosomes 2 and 3 of tomato. Additionally, comparisons with P. trichocarpa and V. vinifera indicated that EgTCP genes have been relatively conserved in these species, with minimal changes in gene copy numbers. These findings suggest that the EgTCP gene family has undergone duplication events, contributing to its evolutionary diversification and functional expansion.

Fig. 4.

Fig. 4

Open in a new tab

Synteny analysis of TCPs

Analysis of cis-regulatory elements in the promoter regions of EgTCP genes

Cis-acting elements play a crucial role in the transcriptional regulation of genes. To better understand the regulatory characteristics of cis-regulatory elements in the promoter regions of EgTCP genes, we extracted 2000 bp upstream sequences from the start codon of each EgTCP gene and analyzed them using the PlantCARE database. The identified cis-regulatory elements were categorized into three major groups: hormone-responsive elements, stress-responsive elements, and elements associated with growth and biological processes. Among these categories, stress-responsive elements were the most abundant (Fig. 5). The promoters of EgTCP genes contained multiple cis-regulatory elements linked to plant stress responses. Notably, the BOX4 element was present in nearly all promoters, with EgTCP14 containing seven BOX4 elements, suggesting that BOX4 plays a key role in the ability of E. grandis to adapt to environmental stress. Within the hormone-responsive elements, ABRE and CGTCA motifs were widely distributed across all EgTCP genes, highlighting the involvement of EgTCP transcription factors in hormone signaling pathways. Interestingly, among the growth- and development-related elements (Fig. 3B), the MYC element was present in the promoters of all EgTCP genes, though the number of MYC motifs varied among family members. Overall, the promoter analysis revealed a diverse and functionally rich set of cis-regulatory elements, suggesting that EgTCP genes play essential roles in stress adaptation, hormone regulation, and plant development.

Fig. 5.

Fig. 5

Open in a new tab

Cis-regulatory element analysis of eucalyptus EgTCPs

3D structural analysis of EgTCP proteins

To investigate the three-dimensional structures of EgTCP proteins, we performed homology modeling using SWISS-MODEL. The 3D structures of all 15 EgTCP proteins were successfully obtained (Fig. 6). The results revealed a high degree of structural similarity within proteins of the same subfamily, with only minor variations. However, when comparing the structures across the CIN, CYC/TB1, and PCF subfamilies, more distinct differences were observed. These structural variations were primarily attributed to differences in the lengths of α-helices, β-turns, and irregular convolutions among the proteins, and we have predicted its structure (Table S1). Notably, most EgTCP proteins contained irregular convolutions, which contribute to variations in spatial folding angles. These findings suggest that structural differences among EgTCP proteins may underlie their distinct functional roles in E. grandis.

Fig. 6.

Fig. 6

Open in a new tab

3D structure prediction of eucalyptus EgTCP proteins

Expression analysis of EgTCP genes under SA, JA, and NaCl stress treatments

To explore the transcriptional responses of EgTCP genes to SA, JA, and NaCl stress, we analyzed gene expression patterns under these treatments (Fig. 7). Under SA treatment (Fig. 7A), EgTCP7 and EgTCP11 exhibited an initial increase in expression followed by a decline, while EgTCP10 and EgTCP13 showed a gradual increase, indicating that their expression is progressively induced by SA. Notably, EgTCP10 and EgTCP13 were also induced by JA, displaying a similar increasing expression trend. Under JA treatment (Fig. 7B), most EgTCP genes showed significant induction at 1 h, 6 h, and 24 h. In particular, EgTCP2, EgTCP4, EgTCP5, EgTCP9, and EgTCP14 exhibited early induction, suggesting their involvement in rapid JA-mediated signaling responses. Under NaCl stress (Fig. 7C), most EgTCP genes showed an initial increase in expression followed by a decline, except for EgTCP2, which displayed a continuous increase. This pattern suggests that EgTCP genes play an essential role in early salt stress responses, with their highest defensive activity occurring within the first 24 h of stress exposure.

Fig. 7.

Fig. 7

Open in a new tab

Expression of eucalyptus EgTCPs under stress conditions. A Expression of EgTCP genes under SA treatment conditions. B Expression of EgTCP genes under JA treatment conditions. C Expression of EgTCP genes under NaCl treatment conditions

Expression analysis of EgTCP genes under phosphorus and boron deficiency

To examine the expression patterns of EgTCP genes under phosphorus (P) and boron (B) deficiency, we analyzed expression profiles in both roots and shoots. In roots, expression analysis on day 21 of phosphorus deficiency treatment (Fig. 8A) revealed that nine genes—EgTCP14, EgTCP4, EgTCP12, EgTCP11, EgTCP15, EgTCP5, EgTCP10, EgTCP13, and EgTCP8—were highly expressed. However, none of these genes were significantly upregulated under boron deficiency, suggesting that root-expressed EgTCP genes respond more actively to phosphorus starvation than to boron deprivation.

Fig. 8.

Fig. 8

Open in a new tab

Expression of eucalyptus EgTCPs under phosphorus and boron deficiency conditions. A Expression of EgTCPs in roots under phosphorus and boron deficiency conditions. B Expression of EgTCPs in shoots under phosphorus and boron deficiency conditions

In contrast, in shoots (Fig. 8B), most EgTCP genes exhibited sensitivity to both phosphorus and boron deficiency. Notably, EgTCP10, EgTCP7, EgTCP12, and EgTCP5 displayed high expression levels at 6 h after phosphorus deficiency treatment, followed by a subsequent decline. This indicates that the primary response to phosphorus starvation in shoots occurs within the early hours of exposure.

Tissue-specific expression patterns of EgTCP genes

To investigate tissue-specific expression patterns of EgTCP genes, we analyzed their expression profiles across different developmental stages and organs. At 30 days of growth (Fig. 9), EgTCP5, EgTCP10, and EgTCP15 exhibited high expression levels in stems, while almost no EgTCP genes showed significant expression in roots, suggesting that EgTCP genes do not play a major role in early root development. During the semiannual growth period of E. grandis, EgTCP4, EgTCP8, EgTCP11, EgTCP13, and EgTCP14 were highly expressed in both young and mature leaves. Nearly all EgTCP genes showed strong expression in the stem apex, indicating that they play critical roles in shoot development during this period. In 3-year-old E. grandis plants, EgTCP genes exhibited high expression in flowers and lateral branches. Notably, EgTCP2 and EgTCP7 were highly expressed in adult leaves, further highlighting their functional specificity in leaf development and differentiation. Overall, the expression analysis revealed that EgTCP genes exhibit significant tissue specificity, with distinct gene members being preferentially expressed in stems, leaves, flowers, and lateral branches during different developmental stages.

Fig. 9.

Fig. 9

Open in a new tab

Expression of the eucalyptus EgTCP gene family in different tissues

Subcellular localization of EgTCP13

EgTCP13 exhibited a significant upregulation trend under SA (salicylic acid) and JA (jasmonic acid) induction conditions. It showed active responses to salt stress across four time points, while demonstrating high expression levels in both young leaves and adult leaves. This leads to the speculation that EgTCP13 may function as a transcription factor regulating stress-responsive pathways. To clarify its subcellular localization, this study utilized a dual fluorescent labeling system for co-localization verification. First, the nuclear marker mCherry fused with a nuclear localization signal (NLS) was employed as a reference, while the target gene EgTCP13 was subcloned into the pCAMBIA1302-GFP vector to construct a GFP fusion expression vector. Following co-transfection of Nicotiana benthamiana leaf epidermal cells via Agrobacterium-mediated transformation, fluorescent signals were captured using confocal laser scanning microscopy (Fig. 10). The results revealed significant spatial overlap (Pearson correlation coefficient > 0.85) between the GFP-EgTCP13 fusion protein (green fluorescence) and the NLS-mCherry nuclear marker (red fluorescence) within the nuclear region. These findings confirm that EgTCP13 possesses definitive nuclear localization properties, and its nuclear distribution pattern aligns with the classical NLS-mediated transport mechanism.

Fig. 10.

Fig. 10

Open in a new tab

Subcellular Localization Analysis of EgTCP13. GFP, Green Fluorescent Protein

Discussion

With the successive publication of plant genome data, the TCP gene family has been systematically identified in multiple species, such as maize (Chai et al. 2017), grape (Leng et al. 2019), and rose (Zou et al. 2023). The release of the E. grandis genome data provides an opportunity for the comprehensive identification of its TCP gene family. In this study, we utilized bioinformatics methods to identify the EgTCP gene family in E. grandis for the first time, identifying a total of 15 EgTCP genes, which is fewer than reported in many other species, such as Arabidopsis, rice, grape, chrysanthemum, and rose have 24, 22, 19, 23, and 18 TCP transcription factors respectively. (Wang et al. 2015; Zou et al. 2023; Tian et al. 2022; Leng et al. 2019; Yin et al. 2018). The difference in the number of TCP genes among different species may be related to the varying degrees of expansion of TCP genes across species. The gene structure of the E. grandis TCP genes is relatively simple, with most members containing only one exon, which is very similar to the TCP gene structures in maize and grape.

Based on the differences in the TCP conserved domains, EgTCP genes are divided into Class I (PCF type) and Class II, with Class II further subdivided into CYC/TB1 and CIN. Phylogenetic analysis indicates that the members of the EgTCP gene family are consistently classified with those reported in other species (Fig. 1). The function of TCP proteins is related to their conserved domains, especially the bHLH domain, which is capable of participating in DNA binding and secondary structure formation (Kosugi and Ohashi 2002). All EgTCP gene family members contain the unique bHLH structure of TCP transcription factors, but there are certain differences in the conserved motifs of different subfamilies. The PCF members contain a greater variety of conserved motifs, with Motif 2 present only in all PCF EgTCPs and Motif 4 found only in the CYC/TB1 and CIN subfamilies. Class I and Class II genes in TCP have opposing functions, with Class I promoting plant growth and cell proliferation, while Class II inhibits plant growth and cell proliferation (Martin-Trillo and Cubas 2010). The differing functions of Class I and Class II TCP genes may be associated with the differences in their conserved motifs (Fig. 2).

EgTCP13 belongs to the CIN sub—family of the TCP gene family. Currently, members of this family are widely involved in the process of photosynthesis. For example, in Arabidopsis thaliana, the hypocotyl elongation of the triple mutant TCP5–TCP13–TCP17 is not affected by shading. In contrast, overexpression of TCP17 leads to hypocotyl elongation both in shaded environments and under white light conditions. TCP17 is a protein with poor stability, and shading can enhance its stability. When plants are transferred from a shaded environment to a white-light environment, TCP17 undergoes degradation, and treatment with the 26S proteasome inhibitor MG132 can inhibit this degradation process. This phenomenon indicates that white light promotes the degradation of TCP17 via the 26S proteasome, while shading inhibits this degradation process. Notably, shading rapidly and reversely regulates the transcription level of TCP17, causing it to decrease (Zhou et al. 2018) This means that the accumulation of TCP17 in shaded environments does not depend on transcriptional regulation but on post-transcriptional regulation.In this study, we also found a similar phenomenon. EgTCP13 is highly expressed in both young and adult leaves but has low expression in other tissues. It is speculated that the function of EgTCP13 is related to photosynthesis. Additionally, this study found that EgTCP13 is localized in the nucleus (Fig. 10), which is similar to the localization of most transcription factors. It is speculated that it performs regulatory functions in the nucleus (Fig. 10).

TCP is a plant-specific transcription factor that is widely involved in various biological processes, including the formation of plant organ morphology, responses to abiotic stress, and hormone regulation (Kolsch and Gleissberg 2006; Damerval et al. 2007; Aguilar-Martinez and Sinha 2013; Seki et al. 2020; Zhao et al. 2021). In Arabidopsis, TCP4 promotes the expression of the LOX2 gene, thereby facilitating the synthesis of jasmonic acid, which inhibits leaf growth (Danisman et al. 2012). AtTCP4 in Arabidopsis is also involved in the regulation of gibberellin-mediated elongation of its hypocotyl (Sarvepalli and Nath 2011). The CIN gene in snapdragon regulates leaf development through cytokinin and auxin pathways. Under high salt conditions, ectopic expression of PeTCP10 from bamboo in Arabidopsis improves the plant’s antioxidant capacity by promoting peroxidase activity and enhances its tolerance to hydrogen peroxide (Xu et al. 2021). BraTCP4-1 in turnip interacts with the WRKYs promoter to activate the expression of pathogen-related genes, increasing resistance to stem rot (Dong et al. 2021). In this study, EgTCP2, EgTCP13, and EgTCP7 showed some homology with AtTCP4 in Arabidopsis. Expression analysis of these three genes indicates that they not only respond to the induction of SA and JA but also actively respond to salt stress.

Conclusion

This study systematically identified and characterized the TCP gene family in E. grandis using whole-genome data. A combined approach involving BLAST and HMMER searches led to the identification of 15 EgTCP genes, which were classified into the PCF, CIN, and CYC/TB1 subfamilies. Comprehensive bioinformatics analyses were conducted, including the assessment of physicochemical properties, gene structures, protein domain compositions, chromosomal distributions, phylogenetic relationships, and promoter elements. Additionally, transcriptome data validated the expression profiles of EgTCP genes across different tissues and under abiotic stress conditions. The collinearity analysis revealed that EgTCP genes are unevenly distributed across chromosomes, with some genes showing evidence of segmental duplication events, suggesting their evolutionary conservation. Promoter analysis identified numerous cis-regulatory elements associated with growth, development, and hormone signaling, further emphasizing the regulatory significance of EgTCP genes. Expression profiling demonstrated that EgTCP genes exhibit distinct tissue-specific expression patterns during leaf development, indicating their involvement in growth regulation. Furthermore, EgTCP genes showed differential responses to stress conditions, such as SA, JA, and NaCl stress, highlighting their potential roles in abiotic stress adaptation in E. grandis. Overall, this study provides a comprehensive foundation for understanding the functional significance of the TCP gene family in E. grandis, paving the way for future research on their roles in plant growth, development, and stress tolerance.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Material 1 (13.6KB, docx)

Author contributions

GP and BZ performed the bioinformatics analysis of the TCP gene family and wrote the manuscript. RX and JH performed the data collation. XY revised the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This Research was Financially Supported by Guangdong Provincial Key Laboratory of Intelligent Port Security Inspection (No. 2023B1212010011).

Data availability

Data will be made available on request.

Declarations

Conflict of interest

The authors declare no conflicts of interest.

Footnotes

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

  1. Aggarwal P, Das GM, Joseph AP, Chatterjee N, Srinivasan N, Nath U (2010) Identification of specific DNA binding residues in the TCP family of transcription factors in Arabidopsis. Plant Cell 22:1174–1189 [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aguilar-Martinez JA, Sinha N (2013) Analysis of the role of Arabidopsis class I TCP genes AtTCP7, AtTCP8, AtTCP22, and AtTCP23 in leaf development. Front Plant Sci 4:406 [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bailey TL, Johnson J, Grant CE, Noble WS (2015) The MEME suite. Nucleic Acids Res 43:W39–W49 [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Braun N, de Saint GA, Pillot JP, Boutet-Mercey S, Dalmais M, Antoniadi I, Li X, Maia-Grondard A, Le Signor C, Bouteiller N, Luo D, Bendahmane A, Turnbull C, Rameau C (2012) The pea TCP transcription factor PsBRC1 acts downstream of strigolactones to control shoot branching. Plant Physiol 158:225–238 [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chai W, Jiang P, Huang G, Jiang H, Li X (2017) Identification and expression profiling analysis of TCP family genes involved in growth and development in maize. Physiol Mol Biol Plants 23:779–791 [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chen C, Wu Y, Li J, Wang X, Zeng Z, Xu J, Liu Y, Feng J, Chen H, He Y, Xia R (2023) TBtools-II: a “one for all, all for one” bioinformatics platform for biological big-data mining. Mol Plant 16:1733–1742 [DOI] [PubMed] [Google Scholar]
  7. Costa ESF, Shvaleva A, Maroco JP, Almeida MH, Chaves MM, Pereira JS (2004) Responses to water stress in two Eucalyptusglobulus clones differing in drought tolerance. Tree Physiol 24:1165–1172 [DOI] [PubMed] [Google Scholar]
  8. Damerval C, Le Guilloux M, Jager M, Charon C (2007) Diversity and evolution of CYCLOIDEA-like TCP genes in relation to flower development in papaveraceae. Plant Physiol 143:759–772 [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Danisman S, van der Wal F, Dhondt S, Waites R, de Folter S, Bimbo A, van Dijk AD, Muino JM, Cutri L, Dornelas MC, Angenent GC, Immink RG (2012) Arabidopsis class I and class II TCP transcription factors regulate jasmonic acid metabolism and leaf development antagonistically. Plant Physiol 159:1511–1523 [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Danisman S, van Dijk AD, Bimbo A, van der Wal F, Hennig L, de Folter S, Angenent GC, Immink RG (2013) Analysis of functional redundancies within the ArabidopsisTCP transcription factor family. J Exp Bot 64:5673–5685 [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Davis G, Kobayashi M, Phinney BO, Lange T, Croker SJ, Gaskin P, MacMillan J (1999) Gibberellin biosynthesis in maize. Metabolic studies with GA(15), GA(24), GA(25), GA(7), and 2,3-dehydro-GA(9). Plant Physiol 121:1037–1045 [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dong W, Ren W, Wang X, Mao Y, He Y (2021) MicroRNA319a regulates plant resistance to Sclerotinia stem rot. J Exp Bot 72:3540–3553 [DOI] [PubMed] [Google Scholar]
  13. Fan C, Lyu M, Zeng B, He Q, Wang X, Lu MZ, Liu B, Liu J, Esteban E, Pasha A, Provart NJ, Wang H, Zhang J (2024) Profiling of the gene expression and alternative splicing landscapes of Eucalyptusgrandis. Plant Cell Environ 47:1363–1378 [DOI] [PubMed] [Google Scholar]
  14. Giraud E, Ng S, Carrie C, Duncan O, Low J, Lee CP, Van Aken O, Millar AH, Murcha M, Whelan J (2010) TCP transcription factors link the regulation of genes encoding mitochondrial proteins with the circadian clock in Arabidopsis thaliana. Plant Cell 22:3921–3934 [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Horn S, Pabon-Mora N, Theuss VS, Busch A, Zachgo S (2015) Analysis of the CYC/TB1 class of TCP transcription factors in basal angiosperms and magnoliids. Plant J 81:559–571 [DOI] [PubMed] [Google Scholar]
  16. Kolsch A, Gleissberg S (2006) Diversification of CYCLOIDEA-like TCP genes in the basal eudicot families Fumariaceae and Papaveraceae s.str. Plant Biol (Stuttg) 8:680–687 [DOI] [PubMed] [Google Scholar]
  17. Kosugi S, Ohashi Y (1997) PCF1 and PCF2 specifically bind to cis elements in the rice proliferating cell nuclear antigen gene. Plant Cell 9:1607–1619 [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kosugi S, Ohashi Y (2002) DNA binding and dimerization specificity and potential targets for the TCP protein family. Plant J 30:337–348 [DOI] [PubMed] [Google Scholar]
  19. Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549 [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Leng X, Wei H, Xu X, Ghuge SA, Jia D, Liu G, Wang Y, Yuan Y (2019) Genome-wide identification and transcript analysis of TCP transcription factors in grapevine. BMC Genomics 20:786 [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Li YC, Lu YC (2019) BLASTP-ACC: parallel architecture and hardware accelerator design for BLAST-based protein sequence alignment. IEEE Trans Biomed Circuits Syst 13:1771–1782 [DOI] [PubMed] [Google Scholar]
  22. Liu MM, Wang MM, Yang J, Wen J, Guo PC, Wu YW, Ke YZ, Li PF, Li JN, Du H (2019) Evolutionary and comparative expression analyses of TCP transcription factor gene family in land plants. Int J Mol Sci 20:3591 [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lopez JA, Sun Y, Blair PB, Mukhtar MS (2015) TCP three-way handshake: linking developmental processes with plant immunity. Trends Plant Sci 20:238–245 [DOI] [PubMed] [Google Scholar]
  24. Luo D, Carpenter R, Vincent C, Copsey L, Coen E (1996) Origin of floral asymmetry in antirrhinum. Nature 383:794–799 [DOI] [PubMed] [Google Scholar]
  25. Ma J, Wang Q, Sun R, Xie F, Jones DC, Zhang B (2014) Genome-wide identification and expression analysis of TCP transcription factors in Gossypium raimondii. Sci Rep 4:6645 [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Madrigal Y, Alzate JF, Pabon-Mora N (2017) Evolution and expression patterns of TCP genes in asparagales. Front Plant Sci 8:9 [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Martin-Trillo M, Cubas P (2010) TCP genes: a family snapshot 10 years later. Trends Plant Sci 15:31–39 [DOI] [PubMed] [Google Scholar]
  28. Matus V, Sanchez MA, Martinez M, Gonzalez B (2003) Efficient degradation of 2,4,6-trichlorophenol requires a set of catabolic genes related to TCP genes from Ralstonia eutropha JMP134(pJP4). Appl Environ Microbiol 69:7108–7115 [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Medhurst JL, Beadle CL (2005) Photosynthetic capacity and foliar nitrogen distribution in Eucalyptusnitens is altered by high-intensity thinning. Tree Physiol 25:981–991 [DOI] [PubMed] [Google Scholar]
  30. Minakuchi K, Kameoka H, Yasuno N, Umehara M, Luo L, Kobayashi K, Hanada A, Ueno K, Asami T, Yamaguchi S, Kyozuka J (2010) FINE CULM1 (FC1) works downstream of strigolactones to inhibit the outgrowth of axillary buds in rice. Plant Cell Physiol 51:1127–1135 [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Nag A, King S, Jack T (2009) miR319a targeting of TCP4 is critical for petal growth and development in Arabidopsis. Proc Natl Acad Sci U S A 106:22534–22539 [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Nishiyama T, Sakayama H, de Vries J, Buschmann H, Saint-Marcoux D, Ullrich KK, Haas FB, Vanderstraeten L, Becker D, Lang D, Vosolsobe S, Rombauts S, Wilhelmsson P, Janitza P, Kern R, Heyl A, Rumpler F, Villalobos L, Clay JM, Skokan R, Toyoda A, Suzuki Y, Kagoshima H, Schijlen E, Tajeshwar N, Catarino B, Hetherington AJ, Saltykova A, Bonnot C, Breuninger H, Symeonidi A, Radhakrishnan GV, Van Nieuwerburgh F, Deforce D, Chang C, Karol KG, Hedrich R, Ulvskov P, Glockner G, Delwiche CF, Petrasek J, Van de Peer Y, Friml J, Beilby M, Dolan L, Kohara Y, Sugano S, Fujiyama A, Delaux PM, Quint M, Theissen G, Hagemann M, Harholt J, Dunand C, Zachgo S, Langdale J, Maumus F, Van Der Straeten D, Gould SB, Rensing SA (2018) The chara genome: Secondary complexity and implications for plant terrestrialization. Cell 174:448–464 [DOI] [PubMed] [Google Scholar]
  33. Pabon-Mora N, Madrigal Y, Alzate JF, Ambrose BA, Ferrandiz C, Wanke S, Neinhuis C, Gonzalez F (2020) Evolution of class II TCP genes in perianth bearing Piperales and their contribution to the bilateral calyx in Aristolochia. New Phytol 228:752–769 [DOI] [PubMed] [Google Scholar]
  34. Parapunova V, Busscher M, Busscher-Lange J, Lammers M, Karlova R, Bovy AG, Angenent GC, de Maagd RA (2014) Identification, cloning and characterization of the tomato TCP transcription factor family. BMC Plant Biol 14:157 [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Ridoutt BG, Pharis RP (1998) Metabolism of deuterium- and tritium-labeled gibberellins in cambial region tissues of Eucalyptus globulus stems. Tree Physiol 18:659–664 [DOI] [PubMed] [Google Scholar]
  36. Sarvepalli K, Nath U (2011) Hyper-activation of the TCP4 transcription factor in Arabidopsis thaliana accelerates multiple aspects of plant maturation. Plant J 67:595–607 [DOI] [PubMed] [Google Scholar]
  37. Seki K, Komatsu K, Tanaka K, Hiraga M, Kajiya-Kanegae H, Matsumura H, Uno Y (2020) A CIN-like TCP transcription factor (LsTCP4) having retrotransposon insertion associates with a shift from Salinas type to Empire type in crisphead lettuce (Lactuca sativa L.). Hortic Res 7:15 [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Shang X, Han Z, Zhang D, Wang Y, Qin H, Zou Z, Zhou L, Zhu X, Fang W, Ma Y (2022) Genome-wide analysis of the TCP gene family and their expression pattern analysis in tea plant (Camelliasinensis). Front Plant Sci 13:840350 [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Tian C, Zhai L, Zhu W, Qi X, Yu Z, Wang H, Chen F, Wang L, Chen S (2022) Characterization of the TCP gene family in chrysanthemum nankingense and the role of CnTCP4 in cold tolerance. Plants (Basel) 11:936 [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Wang C, Feng G, Xu X, Huang L, Nie G, Li D, Zhang X (2023) Genome-wide identification, characterization, and expression of TCP genes family in orchardgrass. Genes (Basel) 14:925 [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Wang H, Ooi BC, Tan KL, Ong TH, Zhou L (2003) BLAST++: BLASTing queries in batches. Bioinformatics 19:2323–2324 [DOI] [PubMed] [Google Scholar]
  42. Wang X, Gao J, Zhu Z, Dong X, Wang X, Ren G, Zhou X, Kuai B (2015) TCP transcription factors are critical for the coordinated regulation of isochorismate synthase 1 expression in Arabidopsis thaliana. Plant J 82:151–162 [DOI] [PubMed] [Google Scholar]
  43. Wang Y, Tang H, Debarry JD, Tan X, Li J, Wang X, Lee TH, Jin H, Marler B, Guo H, Kissinger JC, Paterson AH (2012) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40:e49 [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Xiong W, Zhao Y, Gao H, Li Y, Tang W, Ma L, Yang G, Sun J (2022) Genomic characterization and expression analysis of TCP transcription factors in Setariaitalica and Setariaviridis. Plant Signal Behav 17:2075158 [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Xu S, Luo Y, Cai Z, Cao X, Hu X, Yang J, Luo D (2013) Functional diversity of CYCLOIDEA-like TCP genes in the control of zygomorphic flower development in Lotusjaponicus. J Integr Plant Biol 55:221–231 [DOI] [PubMed] [Google Scholar]
  46. Xu Y, Liu H, Gao Y, Xiong R, Wu M, Zhang K, Xiang Y (2021) The TCP transcription factor PeTCP10 modulates salt tolerance in transgenic Arabidopsis. Plant Cell Rep 40:1971–1987 [DOI] [PubMed] [Google Scholar]
  47. Yin D, Liu X, Shi Z, Li D, Zhu L (2018) An AT-hook protein DEPRESSED PALEA1 physically interacts with the TCP Family transcription factor RETARDED PALEA1 in rice. Biochem Biophys Res Commun 495:487–492 [DOI] [PubMed] [Google Scholar]
  48. Zhao W, Zheng Z, Zhang J, Roger SF, Luo X (2019) Evaluation of the use of eucalyptus to control algae bloom and improve water quality. Sci Total Environ 667:412–418 [DOI] [PubMed] [Google Scholar]
  49. Zhao Y, Su X, Wang X, Wang M, Chi X, Aamir MM, Li G, Cai Y (2021) Comparative genomic analysis of TCP genes in six Rosaceae species and expression pattern analysis in Pyrusbretschneideri. Front Genet 12:669959 [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Zhou Y, Zhang D, An J, Yin H, Fang S, Chu J, Zhao Y, Li J (2018) TCP transcription factors regulate shade avoidance via directly mediating the expression of both phytochrome interacting factors and auxin biosynthetic genes. Plant Physiol 176(2):1850–1861 [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Zou Q, Dong Q, Tian D, Mao L, Cao X, Zhu K (2023) Genome-wide analysis of TCP transcription factors and their expression pattern analysis of rose plants (Rosachinensis). Curr Issues Mol Biol 45:6352–6364 [DOI] [PMC free article] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplementary Material 1 (13.6KB, docx)

Data Availability Statement

Data will be made available on request.

Articles from Physiology and Molecular Biology of Plants are provided here courtesy of Springer

RESOURCES